Transcription-blocking DNA damage in aging: A mechanism for hormesis

BioEssays

Volumn 31, Issue 12, 2009, Pages 1347-1356

  Schumacher, Björn ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Aging; DNA damage; Hormesis; IGF 1; Longevity; Progeroid syndromes; Somatotropic axis; Transcription coupled repair

Indexed keywords

DNA; DNA POLYMERASE; GROWTH HORMONE; GROWTH HORMONE RECEPTOR; INSULIN; LAMIN A; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; RNA POLYMERASE II; SILENT INFORMATION REGULATOR PROTEIN 2; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; SUPEROXIDE DISMUTASE; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR PIT 1;

AEROBIC METABOLISM; AGING; ARTICLE; CANCER PREVENTION; DIET RESTRICTION; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION; GRAVITY; HEAT STRESS; HUMAN; LONGEVITY; NONHUMAN; OXIDATIVE STRESS; POINT MUTATION; PROGERIA; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ADAPTATION, PHYSIOLOGICAL; AGING; ANIMALS; DNA DAMAGE; DNA REPAIR; HUMANS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 73149120015     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.200900107     Document Type: Article

References (99)

1. Schulz H. 1888. Ueber Hefegifte. Pflugers Arch Gesamte Physiol 42: 517-41.
2. Southam CM, Ehrlich J. 1943. Effects of extract of western red-cedar heartwood on certain wood-decaying fungi in culture. Phytopathology 33: 517-24.
3. Calabrese EJ. 2008. Hormesis and medicine. Br J Clin Pharmacol 66: 594-617.
4. Douglas H. 2008. Science, hormesis and regulation. Hum Exp Toxicol 27: 603-7.
5. Kaiser J. 2003. Hormesis. Sipping from a poisoned chalice. Science 302: 376-9.
6. Gems D, Partridge L. 2008. Stress-response hormesis and aging: "that which does not kill us makes us stronger". Cell Metab 7: 200-3.
7. Murakami S. 2006. Stress resistance in long-lived mouse models. Exp Gerontol 41: 1014-9.
8. Cypser JR, Johnson TE. 2003. Hormesis in Caenorhabditis elegans dauer-defective mutants. Biogerontology 4: 203-14.
9. Kirkwood TB. 2005. Understanding the odd science of aging. Cell 120: 437-47.
10. Medawar PB. 1952. An Unsolved Problem of Biology. London: Lewis:
11. Kirkwood TB, Cremer T. 1982. Cytogerontology since 1881: a reappraisal of August Weismann and a review of modern progress. Hum Genet 60: 101-21.
12. Schumacher B, Garinis GA, Hoeijmakers JH. 2008. Age to survive: DNA damage and aging. Trends Genet 24: 77-85.
13. Harman D. 1956. Aging: a theory based on free radical and radiation chemistry. J Gerontol 11: 298-300.
14. Kenyon C, Chang J, Gensch E, et al. 1993. A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-4.
15. Johnson TE. 1990. Increased life-span of age-1 mutants in Caenorhabditis elegans and lower Gompertz rate of aging. Science 249: 908-12.
16. Guarente L, Kenyon C. 2000. Genetic pathways that regulate ageing in model organisms. Nature 408: 255-62.
17. Kenyon C. 2005. The plasticity of aging: insights from long-lived mutants. Cell 120: 449-60.
18. Carter CS, Ramsey MM, Sonntag WE. 2002. A critical analysis of the role of growth hormone and IGF-1 in aging and lifespan. Trends Genet 18: 295-301.
19. Snell GD. 1929. Dwarf, a new Mendelian recessive character of the house mouse. Proc Natl Acad Sci U S A 15: 733-4.
20. Liang H, Masoro EJ, Nelson JF, et al. 2003. Genetic mouse models of extended lifespan. Exp Gerontol 38: 1353-64.
21. Heiman ML, Tinsley FC, Mattison JA, et al. 2003. Body composition of prolactin-, growth hormone, and thyrotropin-deficient Ames dwarf mice. Endocrine 20: 149-54.
22. Bartke A, Brown-Borg H. 2004. Life extension in the dwarf mouse. Curr Top Dev Biol 63: 189-225.
23. Zhou Y, Xu BC, Maheshwari HG, et al. 1997. A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse). Proc Natl Acad Sci U S A 94: 13215-20.
24. Bonkowski MS, Pamenter RW, Rocha JS, et al. 2006. Long-lived growth hormone receptor knockout mice show a delay in age-related changes of body composition and bone characteristics. J Gerontol A Biol Sci Med Sci 61: 562-7.
25. Holzenberger M, Dupont J, Ducos B, et al. 2003. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421: 182-7.
26. Kurosu H, Yamamoto M, Clark JD, et al. 2005. Suppression of aging in mice by the hormone Klotho. Science 309: 1829-33.
27. Spindler SR. 2005. Rapid and reversible induction of the longevity, anticancer and genomic effects of caloric restriction. Mech Ageing Dev 126: 960-6.
28. Partridge L, Pletcher SD, Mair W. 2005. Dietary restriction, mortality trajectories, risk and damage. Mech Ageing Dev 126: 35-41.
29. Partridge L, Gems D. 2002. Mechanisms of ageing: public or private? Nat Rev Genet 3: 165-75.
30. Bartke A, Wright JC, Mattison JA, et al. 2001. Extending the lifespan of long-lived mice. Nature 414: 412.
31. Bonkowski MS, Rocha JS, Masternak MM, et al. 2006. Targeted disruption of growth hormone receptor interferes with the beneficial actions of calorie restriction. Proc Natl Acad Sci U S A 103: 7901-5.
32. Guarente L, Picard F. 2005. Calorie restriction-the SIR2 connection. Cell 120: 473-82.
33. Sinclair DA, Guarente L. 1997. Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91: 1033-42.
34. Wang Y, Tissenbaum HA. 2006. Overlapping and distinct functions for a Caenorhabditis elegans SIR2 and DAF-16/FOXO. Mech Ageing Dev 127: 48-56.
35. Tissenbaum HA, Guarente L. 2001. Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410: 227-30.
36. Greiss S, Hall J, Ahmed S, et al. 2008. C. elegans SIR-2.1 translocation is linked to a proapoptotic pathway parallel to cep-1/p53 during DNA damage-induced apoptosis. Genes Dev 22: 2831-42.
37. Guarente L. 2006. Sirtuins as potential targets for metabolic syndrome. Nature 444: 868-74.
38. Baur JA, Pearson KJ, Price NL, et al. 2006. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337-42.
39. Mostoslavsky R, Chua KF, Lombard DB, et al. 2006. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 124: 315-29.
40. Oberdoerffer P, Michan S, McVay M, et al. 2008. SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging. Cell 135: 907-18.
41. Levine AJ, Feng Z, Mak TW, et al. 2006. Coordination and communication between the p53 and IGF-1-AKT-TOR signal transduction pathways. Genes Dev 20: 267-75.
42. Stanfel MN, Shamieh LS, Kaeberlein M, et al. 2009. The TOR pathway comes of age. Biochim Biophys Acta.
43. Harrison DE, Strong R, Sharp ZD, et al. 2009. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature.
44. Shanley DP, Kirkwood TB. 2006. Caloric restriction does not enhance longevity in all species and is unlikely to do so in humans. Biogerontology 7: 165-8.
45. Colman RJ, Anderson RM, Johnson SC, et al. 2009. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325: 201-4.
46. Harper JM, Salmon AB, Leiser SF, et al. 2007. Skin-derived fibroblasts from long-lived species are resistant to some, but not all, lethal stresses and to the mitochondrial inhibitor rotenone. Aging Cell 6: 1-13.
47. Leiser SF, Salmon AB, Miller RA. 2006. Correlated resistance to glucose deprivation and cytotoxic agents in fibroblast cell lines from long-lived pituitary dwarf mice. Mech Ageing Dev 127: 821-9.
48. Salmon AB, Murakami S, Bartke A, et al. 2005. Fibroblast cell lines from young adult mice of long-lived mutant strains are resistant to multiple forms of stress. Am J Physiol Endocrinol Metab 289: E23-9.
49. Johnson TE, Henderson S, Murakami S, et al. 2002. Longevity genes in the nematode Caenorhabditis elegans also mediate increased resistance to stress and prevent disease. J Inherit Metab Dis 25: 197-206.
50. Wolff S, Ma H, Burch D, et al. 2006. SMK-1, an essential regulator of DAF-16-mediated longevity. Cell 124: 1039-53.
51. Neumann-Haefelin E, Qi W, Finkbeiner E, et al. 2008. SHC-1/p52Shc targets the insulin/IGF-1 and JNK signaling pathways to modulate life span and stress response in C. elegans. Genes Dev 22: 2721-35. 52. Rea SL, Wu D, Cypser JR, et al. 2005. A stress-sensitive reporter predicts longevity in isogenic populations of Caenorhabditis elegans. Nat Genet 37: 894-8.
52. Landis GN, Abdueva D, Skvortsov D, et al. 2004. Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proc Natl Acad Sci U S A 101: 7663-8.
53. Doonan R, McElwee JJ, Matthijssens F, et al. 2008. Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev 22: 3236-41.
54. Melov S, Ravenscroft J, Malik S, et al. 2000. Extension of life-span with superoxide dismutase/catalase mimetics. Science 289: 1567-9.
55. Hasty P, Campisi J, Hoeijmakers J, et al. 2003. Aging and genome maintenance: lessons from the mouse? Science 299: 1355-9.
56. Ramirez CL, Cadinanos J, Varela I, et al. 2007. Human progeroid syndromes, aging and cancer: new genetic and epigenetic insights into old questions. Cell Mol Life Sci 64: 155-70.
57. Lombard DB, Chua KF, Mostoslavsky R, et al. 2005. DNA repair, genome stability, and aging. Cell 120: 497-512.
58. Sinclair DA, Oberdoerffer P. 2009. The ageing epigenome: damaged beyond repair? Ageing Res Rev 8: 189-98.
59. Hoeijmakers JH. 2001. Genome maintenance mechanisms for preventing cancer. Nature 411: 366-74.
60. Bartek J, Lukas J. 2007. DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19: 238-45.
61. Sedelnikova OA, Horikawa I, Zimonjic DB, et al. 2004. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat Cell Biol 6: 168-70.
62. Caspari T, Carr AM. 1999. DNA structure checkpoint pathways in Schizosaccharomyces pombe. Biochimie 81: 173-81.
63. Foiani M, Pellicioli A, Lopes M, et al. 2000. DNA damage checkpoints and DNA replication controls in Saccharomyces cerevisiae. Mutat Res 451: 187-96.
64. Harrison JC, Haber JE. 2006. Surviving the breakup: the DNA damage checkpoint. Annu Rev Genet 40: 209-35.
65. Campisi J. 2005. Aging, tumor suppression and cancer: high wire-act! Mech. Ageing Dev 126: 51-8.
66. Vogelstein B, Lane D, Levine AJ. 2000. Surfing the p53 network. Nature 408: 307-10.
67. Abraham RT. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 15: 2177-96.
68. Bartek J, Lukas J. 2003. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3: 421-9.
69. Meier UT. 2003. Dissecting dyskeratosis. Nat Genet 33: 116-7.
70. Marrone A, Walne A, Dokal I. 2005. Dyskeratosis congenita: telomerase, telomeres and anticipation. Curr Opin Genet Dev 15: 249-57.
71. Liu B, Wang J, Chan KM, et al. 2005. Genomic instability in laminopathybased premature aging. Nat Med 11: 780-5.
72. Shiloh Y. 1997. Ataxia-telangiectasia and the Nijmegen breakage syndrome: related disorders but genes apart. Annu Rev Genet 31: 635-62.
73. Gurtan AM, D'Andrea AD. 2006. Dedicated to the core: understanding the Fanconi anemia complex. DNA Repair (Amst) 5: 1119-25.
74. Niedernhofer LJ, Lalai AS, Hoeijmakers JH. 2005. Fanconi anemia (cross)linked to DNA repair. Cell 123: 1191-8.
75. Lehmann AR. 2003. DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 85: 1101-11.
76. Mitchell JR, Hoeijmakers JH, Niedernhofer LJ. 2003. Divide and conquer: nucleotide excision repair battles cancer and ageing. Curr Opin Cell Biol 15: 232-40.
77. Ljungman M, Lane DP. 2004. Transcription - guarding the genome by sensing DNA damage. Nat Rev Cancer 4: 727-37.
78. Essers J, van Cappellen WA, Theil AF, et al. 2005. Dynamics of relative chromosome position during the cell cycle. Mol Biol Cell 16: 769-75.
79. Garinis GA, Mitchell JR, Moorhouse MJ, et al. 2005. Transcriptome analysis reveals cyclobutane pyrimidine dimers as a major source of UVinduced DNA breaks. EMBO J 24: 3952-62.
80. Bohr VA, Smith CA, Okumoto DS, et al. 1985. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40: 359-69.
81. You YH, Lee DH, Yoon JH, et al. 2001. Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells. J Biol Chem 276: 44688-94.
82. Niedernhofer LJ, Garinis GA, Raams A, et al. 2006. A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 444: 1038-43.
83. van der Pluijm I, Garinis GA, Brandt RM, et al. 2006. Impaired genome maintenance suppresses the growth hormone-insulin-like growth factor 1 axis in mice with Cockayne syndrome. PLoS Biol 5: e2.
84. Schumacher B, van der Pluijm I, Moorhouse MJ, et al. 2008. Delayed and accelerated aging share common longevity assurance mechanisms. PLoS Genet 4: e1000161.
85. Wijnhoven SW, Hoogervorst EM, de Waard H, et al. 2007. Tissue specific mutagenic and carcinogenic responses in NER defective mouse models. Mutat Res 614: 77-94.
86. Wijnhoven SW, Beems RB, Roodbergen M, et al. 2005. Accelerated aging pathology in ad libitum fed Xpd(TTD) mice is accompanied by features suggestive of caloric restriction. DNA Repair (Amst) 4: 1314-24.
87. Susa D, Mitchell JR, Verweij M, et al. 2009. Congenital DNA repair deficiency results in protection against renal ischemia reperfusion injury in mice. Aging Cell 8: 192-200.
88. Garinis GA, Uittenboogaard LM, Stachelscheid H, et al. 2009. Persistent transcription-blocking DNA lesions trigger somatic growth attenuation associated with longevity. Nat Cell Biol 11: 604-15.
89. Rivera EJ, Goldin A, Fulmer N, et al. 2005. Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine. J Alzheimers Dis 8: 247-68.
90. Li M, Li C, Parkhouse WS. 2003. Age-related differences in the des IGFI-mediated activation of Akt-1 and p70 S6K in mouse skeletal muscle. Mech Ageing Dev 124: 771-8.
91. Jaspers NG, Raams A, Kelner MJ, et al. 2002. Anti-tumour compounds illudin S and Irofulven induce DNA lesions ignored by global repair and exclusively processed by transcription- and replication-coupled repair pathways. DNA Repair (Amst) 1: 1027-38.
92. Dianov GL, Parsons JL. 2007. Co-ordination of DNA single strand break repair. DNA Repair (Amst) 6: 454-60.
93. DiBiase SJ, Zeng ZC, Chen R, et al. 2000. DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res 60: 1245-53.
94. Dizdaroglu M. 2005. Base-excision repair of oxidative DNA damage by DNA glycosylases. Mutat Res 591: 45-59.
95. Charlet-Berguerand N, Feuerhahn S, Kong SE, et al. 2006. RNA polymerase II bypass of oxidative DNA damage is regulated by transcription elongation factors. EMBO J 25: 5481-91.
96. Larsson O, Girnita A, Girnita L. 2005. Role of insulin-like growth factor 1 receptor signalling in cancer. Br J Cancer 92: 2097-101.
97. Hartog H, Wesseling J, Boezen HM, et al. 2007. The insulin-like growth factor 1 receptor in cancer: old focus, new future. Eur J Cancer 43: 1895-904.
98. Garinis GA, Schumacher B. 2009. Transcription-blocking DNA damage in aging and longevity. Cell Cycle 8.
99. Bartke A. 2009. The somatotropic axis and aging: mechanisms and persistent questions about practical implications. Exp Gerontol 44: 372-4.